Accurate sound localization is based on three acoustic cues (interaural time and intensity difference and spectral cues from directional filtering by the pinna). In natural listening conditions, every spatial position of a sound source provides a unique combination of these three cues in "natural alignment." Although neurons in the central nucleus (ICC) of the inferior colliculus (IC) are sensitive to multiple cues, they do not favor their natural spatial alignment. We tested for sensitivity to cue alignment in the nucleus of the brachium of the IC (BIN) in unanesthetized marmoset monkeys. The BIN receives its predominant auditory input from ICC and projects to the topographic auditory space map in the superior colliculus. Sound localization cues measured in each monkey were used to synthesize broadband stimuli with aligned and misaligned cues; spike responses to these stimuli were recorded in the BIN. We computed mutual information (MI) between the set of spike rates and the stimuli containing either aligned or misaligned cues. The results can be summarized as follows: 1) BIN neurons encode more information about auditory space when cues are aligned compared with misaligned. 2) Significantly more units prefer aligned cues in the BIN than in ICC. 3) An additive model based on summing the responses to stimuli with the localization cues varying individually accurately predicts the alignment preference with all cues varying. Overall, the results suggest that the BIN is the first site in the ascending mammalian auditory system that is tuned to natural combinations of sound localization cues.